Response of cultured Microcystis aeruginosa from the Swan River, Australia, to elevated salt concentration and consequences for bloom and toxin management in estuaries
Philip T. Orr A D E , Gary J. Jones A C and Grant B. Douglas BA CSIRO Land and Water, 120 Meiers Road, Indooroopilly, Qld 4068, Australia.
B CSIRO Land and Water, Centre for Environment and Life Sciences, Underwood Avenue, Floreat, WA 6014, Australia.
C Present address: CRC Freshwater Ecology, University of Canberra, Belconnen, ACT 2610, Australia.
D Present address: 3 Urmia Close, Westlake, Qld 4074, Australia.
E Corresponding author. Email: philip.orr@bigfoot.com
Marine and Freshwater Research 55(3) 277-283 https://doi.org/10.1071/MF03164
Submitted: 26 September 2003 Accepted: 12 March 2004 Published: 19 May 2004
Abstract
A mixed bloom of Microcystis aeruginosa forma aeruginosa and forma flos-aquae from the Swan River, Western Australia, was confirmed toxic by HPLC analysis. At least four, and possibly 11, microcystins were detected in cell-free extracts. Live bloom material was cultured at salt concentrations up to 21.2 g L–1 (total salts). The cultures were salt tolerant up to 9.8 g L–1. Reduction in the total cell concentration in the first 23 h was only observed in the highest salt treatment and first-order rate constants for cell lysis were higher than the rates for reduction of the intracellular microcystin pool size for that treatment. This suggests preferential lysis of genotypes with lower salinity tolerance and toxigenicity. This increased the toxicity of the mixed bloom population and the apparent microcystin cell quota without any change to the intracellular microcystin pool size. Therefore, the toxicity of bloom material may change through preferential lysis of cells with lower tolerances to changing environmental conditions, including salinity. Managers should be aware that the World Health Organization alert levels of 105 cells mL–1 for human contact exposure to cyanobacteria may not be a suitable prima facie test during these periods.
Extra keywords: cyanotoxins, high-performance liquid chromatography, HPLC, microcystin, Perth, toxicity.
Acknowledgments
The authors thank Ms Cheryl Orr for expert technical assistance in maintaining and sampling the cultures, for HPLC sample preparation and cell counting. We thank Dr Ingrid Chorus, Dr Susan Blackburn, and two unknown referees for reviewing our manuscript and suggesting useful changes. The Waters and Rivers Commission of Western Australia provided the financial support for this study. We thank them, and in particular Mr Malcolm Robb, for that support.
Armitage, P. (1980). (Blackwell Scientific Publications: Oxford, UK.)
Atkins, R. , Rose, T. , Brown, R. S. , and Robb, M. (2001). The Microcystis cyanobacterial bloom in the Swan River: February 2001. Water Science and Technology 43, 107–114.
| PubMed |
Baker, P. D., and Fabbro, L. D. (1999). (Cooperative Research Centre for Freshwater Ecology: Albury.)
Berg, K. , Skulberg, O. M. , and Skulberg, R. (1987). Effects of decaying toxic blue–green algae on water quality: a laboratory study. Archiv für Hydrobiologie 108, 549–563.
Bourne, D. G. , Jones, G. J. , Blakeley, A. , Jones, A. , Negri, A. P. , and Riddles, P. (1996). Enzymatic pathway for the bacterial degradation of the cyanobacterial cyclic peptide toxin microcystin LR. Applied and Environmental Microbiology 62, 4086–4094.
| PubMed |
Chorus, I., and Bartram, J. (1999). (E&FN Spon (for the World Health Organization): London, UK.)
Humphries, S. E. , and Widjaja, F. (1979). A simple method for separating cells of Microcystis aeruginosa for counting. British Phycological Journal 14, 313–316.
Jähnichen, S. , Petzoldt, T. , and Benndorf, J. (2001). Evidence for control of microcystin dynamics in Bautzen Reservoir (Germany) by cyanobacterial population growth rates and dissolved inorganic carbon. Archiv für Hydrobiologie 150, 177–196.
Jones, G. J. , and Orr, P. T. (1994). Release and degradation of microcystin following algicide treatment of a Microcystis aeruginosa bloom in a recreational lake, as determined by HPLC and protein phosphatase inhibition assay. Water Research 28, 871–876.
| Crossref | GoogleScholarGoogle Scholar |
Jones, G. J. , Bourne, D. G. , Blakely, R. L. , and Hörst, D. (1994). Degradation of the cyanobacterial hepatotoxin microcystin by aquatic bacteria. Natural Toxins 2, 228–235.
| PubMed |
Jones, G. J. , Falconer, I. F. , and Wilkins, R. M. (1995). Persistence of cyclic peptide toxins in dried cyanobacterial crusts from Lake Mokoan, Australia. Environmental Toxicology and Water Quality 10, 19–24.
Kenefick, S. L. , Hrudey, S. E. , Peterson, H. G. , and Prepas, E. E. (1993). Toxin release from Microcystis aeruginosa after chemical treatment. Water Science and Technology 27, 433–440.
Kiviranta, J. , Sivonen, K. , Lahti, K. , Luukkainen, R. , and Niemelä, S. I. (1991). Production and biodegradation of cyanobacterial toxins: a laboratory study. Archiv für Hydrobiologie 121, 281–294.
Long, B. M. , Jones, G. J. , and Orr, P. T. (2001). Cellular microcystin content in N-limited Microcystis aeruginosa can be predicted from growth rate. Applied and Environmental Microbiology 67, 278–283.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
NHMRC (2001). (National Health and Medical Research Council and the Agricultural Resource Management Council of Australia and New Zealand: Canberra, Australia.)
Nikulina, V. N. (2003). Seasonal dynamics of phytoplankton in the inner Neva Estuary in the 1980s and 1990s. Oceanologia 45, 25–39.
Orr, P. T. , and Jones, G. J. (1998). Relationship between microcystin production and cell division rates in nitrogen-limited Microcystis aeruginosa cultures. Limnology and Oceanography 43, 1604–1614.
Otsuka, S. , Suda, S. , Li, R. , Watanabe, M. , Oyaizu, H. , Matsumoto, S. , and Watanabe, M. M. (1999). Characterization of morphospecies and strains of the genus Microcystis (Cyanobacteria) for a reconsideration of species classification. Phycological Research 47, 189–197.
| Crossref | GoogleScholarGoogle Scholar |
Robson, B. J. , and Hamilton, D. P. (2002). Three-dimensional modelling of a Microcystis bloom event in a Western Australian estuary. Proceedings of the International Environmental Modelling and Software Society 3, 491–496.
Rocha, C. , Galvão, H. , and Barbosa, A. (2002). Role of transient silicon limitation in the development of cyanobacteria blooms in the Guadiana estuary, south-western Iberia. Marine Ecology Progress Series 228, 35–45.
Sellner, K. G. , Lacouture, R. V. , and Parrish, C. R. (1988). Effects of increasing salinity on a cyanobacteria bloom in the Potomac estuary. Journal of Plankton Research 10, 49–61.
Sivonen, K. (1985). Effects of light, temperature, nitrate, orthophosphate, and bacteria on growth of and hepatotoxin production by Oscillatoria agardhii strains. Applied and Environmental Microbiology 56, 2658–2666.
Stein, J. R. (1973). (Cambridge University Press: Cambridge, UK.)
Thompson, P. A., Adeney, J. and Gerritse, R. (1997). Phytoplankton in the Swan River: research results 1993 to 1996 and management implications. In (Ed J. R. Davis) pp. 1–14. (CSIRO Land and Water: Canberra.)
Thompson, P. A. , Waite, A. M. , and McMahon, K. (2003). Dynamics of a cyanobacterial bloom in a hypereutrophic, stratified weir pool. Marine and Freshwater Research 54, 27–37.
| Crossref | GoogleScholarGoogle Scholar |
Wicks, R. J. , and Thiel, P. G. (1990). Environmental factors affecting the production of peptide toxins in floating scums of the cyanobacterium Microcystis aeruginosa in a hypertrophic African reservoir. Environmental Science and Technology 24, 1413–1418.